Pancreatic Tuberculosis: An Overview

JOP. J Pancreas (Online) 2015 May 20; 16(3):232-238.
REVIEW ARTICLE
Pancreatic Tuberculosis: An Overview
Shabnam Shahrokh, Mohammad Bagher Miri, Mohammad Taghi Safari,
Amir Houshang Mohammad Alizadeh
Research Center for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical
Sciences, Taleghani Hospital, Tehran, Iran
ABSTRACT
Pancreatic tuberculosis is a rare occurrence in either immune-competent or immune-suppressed host. Pancreatic tuberculosis most commonly afflicts the region of the head and the uncinate process of the pancreas. It is often misdiagnosed due to low index of suspicion and
masquerading of its symptoms as more common pancreatic conditions such as pancreatic malignancy. However, Endoscopic ultrasound
fine needle aspiration sampling with an acid-fast smear is essential for establishing the diagnosis of pancreatic tuberculosis. If the diagnosis is delayed, pancreatic tuberculosis can be fatal. Pancreatic tuberculosis responds well to standard anti-tuberculous drugs.
Introduction
Tuberculosis (TB) is a serious health problem worldwide
[1]. It is a multi-systemic bacterial infection caused by
different strains of mycobacteria, usually Mycobacterium
tuberculosis. It occurs in nearly 9.7 million people [2, 3],
and claims about 2 million lives each year worldwide [4]
highest incidence being in Asia, South America, Eastern
Europe, and most sub-Saharan African countries [2, 3].
Although the incidence of TB was low in developed
countries, it has risen in recent years due to an increase
in emigration from tuberculosis- endemic areas, the
emergence of human immunodeficiency virus (HIV)
infection [5], and widespread use of immunosuppressant
drugs [6, 7]. For example Australia, Western Pacific and
South East Asia have incidence rates of 5-6, 108, 181 per
population, respectively [8, 9] and United States Center
for Disease Control and Prevention (CDC) reported
approximately 11200 new cases of TB in 2014 [10].
Although TB usually involves lungs, extra-pulmonary TB
(EPTB) accounts for nearly 10-30% (approximately 1520%) of all cases of TB in immunocompetent hosts [3,
11, 12]. About 12.5% of all TB cases have EPTB [13] who
nearly 50 percent of them are human immunodeficiency
virus (HIV)-positive [14, 15].
By definition, EPTB is when TB occurs at sites other than
the lung. It can occur in almost any organ system; most
commonly in the lymph nodes, pleura, genitourinary
Received February 24th, 2015- Accepted March 28th, 2015
Keywords Pancreas
Correspondence Amir Houshang Mohammad Alizadeh
Shahid Beheshti University of Medical Sciences
Talegani Hospital, Parvaneh Ave, Tabnak
St, Evin, Tehran, Iran. 19857
Phone +0098-21-22432521
Fax +0098-21-22432517
E-mail ahmaliver@yahoo.com
system, and bone [14, 15]. Note that EPTB must not be
confused with miliary TB, as miliary refers to EPTB with
pulmonary involvement, and not EPTB in isolation [16].
Abdominal TB is a common site for EPTB [15]. It accounts
for 5-12% of patients with tuberculosis (with the
highest prevalence in developing countries) [17, 18] and
almost 11-16% of patients with EPTB have abdominal
involvement [13]. Abdominal TB includes infection of
different combinations of gastrointestinal tract (especially
ileocecal region), lymph nodes, peritoneum, and intraabdominal organs such as the spleen, liver, and pancreas
[15, 19-29].
Pancreatic tuberculosis, either with or without peripancreatic lymphadenitis, is a rare occurrence in either
immunocompetent or immunosuppressed host. It was
first reported by Auerbach in 1944. In his series of 1656
autopsies of tuberculous patients, only 14 cases had
pancreatic involvement that may have mimicked neoplasia
but he did not find any cases of isolated pancreatic
tuberculosis [28]. Pancreatic tuberculosis usually occurs
in patients with miliary tuberculosis with pulmonary
and extra-pulmonary involvement including pancreas, or
in isolated EPTB cases without pulmonary involvement
especially in acquired immunodeficiency syndrome
(0.46%) [13, 14, 21, 23, 27, 28, 30, 31]. But even HIVinfected patients have an incidence of 0.46% [32, 33].
Autopsy studies have shown that the pancreas is involved
in 2.1%–4.7% of patients with miliary tuberculosis [28,
34-38]. However, in a study from 1999-2004 from India
detected pancreatic TB in 8.3% of the 384 patients who
were diagnosed with abdominal TB [39].
As mentioned above, pancreatic tuberculosis is occasionally
observed in people with other organ's involvement as a
consequence of miliary TB or EPTB with involvement of
other organs in addition to pancreas [28, 34]. But primary
pancreatic tuberculosis (PPTB) is described as an isolated
involvement of pancreas by mycobacterium tuberculosis
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JOP. J Pancreas (Online) 2015 May 20; 16(3):232-238.
in the absence of involvement of any other organ or
previously identified TB [36]. PPTB is particularly rare [37,
38]; fewer than 100 cases have been reported worldwide
[39] and its incidence is estimated to be less than 4.7%
[28, 31]. Bhansali in a series of 300 miliary tuberculosis
patients over 12 years in India, did not reveal even 1 with
pancreatic involvement [2, 10, 15, 21].
Isolated pancreatic TB is predominantly observed in the
following patient types:
•
Patients who reside in endemic tuberculose zones,
•
Patients who are immuno-compromised [40]
•
Patients in areas of widespread TB dissemination such
as a military setting and developing countries [19, 20,
25, 27],
However pancreatic TB has also been reported with
increased frequency from western world [41] and the
reported number of such cases in immunocompetent
patients has increased over the past decade [31]. This
increasing incidence is probably due to globalization,
increased use of immunosuppressants, the worldwide
resurrection of M. tuberculosis and the HIV pandemic [31,
34, 42, 43].
A recent review reported that 23% of the 62 cases of
pancreatic TB occurred in patients who were HIV infected
[44]. In AIDS cases, tuberculous pancreatic abscesses are
most common, accounting for 70.0% of cases. In addition,
71.1% of cases have no previous serological evidence
of HIV infection, and 76.2% of patients are severely
immunocompromised hosts with a CD4 cell count of ≤190/
mm3 [5, 29, 45].
More than half of patients with pancreas tuberculosis in
the world literature are young adults (<30 years old) [39,
46]. Convincing epidemiological data with regards to sex
are conflicting, suggesting that pancreatic TB is more
common in men [27, 39].
Pancreatic TB most commonly afflicts the region of the
head and the uncinate process of the pancreas [47, 48]. It
is often misdiagnosed due to low index of suspicion and
masquerading of its symptoms as more common pancreatic
conditions such as pancreatic malignancy [36, 47, 49]. If
the diagnosis is delayed, pancreatic TB can be fatal; it has
a 10.8% mortality rate (comparing to the mortality rate
of 9.1% in immunocompetent patients) [50]. However,
pancreatic TB responds well to standard antituberculous
drugs (ATDs).
Pathogenesis
Because of its rarity, the pathogenesis of pancreatic/
peri-pancreatic involvement of TB is not known with
certainty and it is not yet clear how the infection can only
affect the pancreas [51, 52]. It is believed that this low
frequency is due to retroperitoneal location of pancreas
as well as pancreatic enzymes including lipases and
deoxyribonucleases that interfere with the colonization,
seeding and proliferation of the bacteria [4, 38, 53, 54].
Pancreatic secretions also showed an antitubercular effect
in vitro [51, 52], thus a large intrapancreatic inoculum
of Mycobacterium tuberculosis is required to cause
pancreatic lesions [53, 55].
Although the primary site of TB is usually not evident
in most cases of hepatobiliary and pancreatic TB [56],
several possible mechanisms for pancreatic involvement
of tuberculosis have been discussed. Ingestion of infected
material from an active pulmonary lesion is one. Following
ingestion the bacilli gain access to the gastrointestinal
tract where necrotizing granulomas may develop and then
spread to the lymphatics affecting any organ in the GI tract,
including hepatobiliary and pancreatic tissue [57]. Other
mechanisms include lymphohematogenous dissemination
from pulmonary disease, reactivation of latent tuberculosis
in the pancreatic focus and toxic-allergic reaction of
the pancreas involving an inflammatory response to
generalized tuberculosis [19, 28, 37, 56, 58, 59].
Clinical Features
Over the last two years, 39 patients with pancreatic
tuberculosis were reported in the literature. Of these
patients, 26 were males and age ranged from 13 to 58
years. The outstanding signs and symptoms of pancreatic
tuberculosis are summarized as Table 1. Most common
location of pancreatic tuberculosis as a mass has been
reported in the head (29-74.4%) followed by body (717.9%), uncinate (3-7.7%), and tail (2-5.1%). Abdominal
pain is the most common (31-79.5%) symptom followed
by fever (20-51.3%), weight loss (19-48.7%), appetite loss
(11-28.2%), and jaundice (8-20.5%) that were obstructive
in nature.
Three patients had the past history of pulmonary
tuberculosis and lymphadenopathy was present in 22
patients. Pancreatic tuberculosis leaded to local vascular
invasion in 10 patients also causing diagnostic confusion
with locally advanced or metastatic pancreatic malignancy.
Portal vein, superior mesenteric vein and hepatic artery
involvement were reported in 6 (15.4%), 4 (10.3%), and 4
(10.3%) patients, respectively.
Diagnosis
Diagnosing pancreatic TB is challenging due to its
nonspecific clinical, laboratory or radiological features.
Since pancreatic TB may present as cystic or solid pancreatic
masses, abscesses, lymphomas, pseudocysts or acute or
chronic pancreatitis, cytological or histopathological as
well as bacteriological confirmation is necessary for the
diagnosis of pancreatic tuberculosis.
Pancreatic tuberculosis is a potential mimic of pancreatic
malignancy. Although local vascular invasion is often
considered to be an imaging feature of malignant
lesions, the presence of vascular invasion cannot exclude
possibility of pancreatic tuberculosis [60]. Also, the
dilation of the pancreatic main or branch duct does not
distinguish one condition from the other. However, there
was other evidence against pancreatic malignancy such
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Table 1. Summary of reported cases of pancreatic tuberculosis over the last two years.
Age (yr)/
sex
Location
Presenting symptoms
Rana et al. [92]
28/male
Head and body
Abdominal pain, appetite
loss, weight loss
Cystic
40/female
Head
Abdominal pain, jaundice,
appetite loss, weight loss
Cystic
32/male
Head and uncinate
34/male
Head and body
Abdominal pain, jaundice,
appetite loss, weight loss
26/male
Head
34/male
Head and uncinate
Abdominal pain, jaundice,
appetite loss, weight loss
Yang et al. [93]
40/male
28/male
Rana et al. [79]
Santhosh et al. [55]
Huang et al. [61]
Falkowski et al. [62]
Vafa et al. [41]
43/male
Head
Abdominal pain, appetite
loss, weight loss
Abdominal pain, jaundice,
appetite loss, weight loss
Abdominal pain, pruritus,
jaundice, appetite loss,
weight loss
Para-ancreatic
15/male
Head
Head
Head
58/male
15/male
34/female
Tail
Head
Peripancreatic
Present
Present
None
Abdominal pain, weight loss
Cyctic
Abdominal pain, weight loss
Abdominal pain, jaundice
Abdominal pain, Bilious
vomiting
Abdominal pain, dyspepsia
Abdominal pain
Anorexia, fever, weight
loss, pain and lump in
epigastrium
Fever, vitiligo
Fever, pain and lump in
epigastrium
Anorexia, fever, weight loss
Fever, weight loss, pain and
lump in epigastrium
Present
Absent
Head
Anorexia, fever and pain in
epigastrium
fever and pain in
epigastrium
Normal
Common bile duct dilation
None
Normal
None
None
Normal
Normal
Bile Duct dilatation
Present
Duodenum, portal vein
Absent
Right lobe of liver
Pancreatic and common bile
duct dilatation
Cyctic
Present
-
Cyctic
Absent
Cyctic
Cyctic
Cyctic
Cyctic
Cyctic
Cyctic
Cyctic
Present
Absent
Absent
Present
Cyctic
Cyctic
Cyctic
None
-
-
-
Absent
-
Absent
Present
Absent
Solid Cyctic
Present
Solid Cyctic
Absent
Solid –
Cyctic
Portal vein
Absent
Present
37/male
Normal
Biliary radicles and bile duct
dilatation
Cyctic
Fever and pain in
epigastrium
Normal
Normal
Portal vein, splenic artery,
hepatic artery
Present
Fever, numbness in both
lower limbs, weakness
Normal
Absent
Cyctic
Cyctic
Anorexia, fever
Fever, weight loss
Epigastric pain, fever,
weight loss
Head
Absent
Cyctic
Peripancreatic
35/male
Cyctic
Present
Fever and tail mass,
jaundice
31/male
Peripancreatic
Solid
Cyctic
fever, pain in epigastrium
28/female
Normal
Cyctic
Solid
Abdominal pain
Peripancreatic
Head
Normal
Present
45/male
27/male
Present
Solid
Head
Head
Common bile duct and
intrahepatic biliary radicles
dilation
Normal
40/male
51/male
Normal
Weight loss, fever, night
sweat
Peripancreatic
Peripancreatic
Present
Normal
Normal
Abdominal pain
44/female
45/female
Solid
Portal vein
Absent
Abdominal pain, weight loss
Head and body
Head
Absent
Common bile duct obstruction
36/male
34/male
Pancreatic duct dilatation
Cystic
Portal vein, superior
mesenteric vein and artery,
hepatic artery
Normal
Head and uncinate
Head and body
Present
Normal
Absent
45/female
28/female
Cystic
Superior mesenteric Vein
Cystic
Abdominal pain, jaundice
Head
Present
Normal
Abdominal pain, weight
loss, fever
Head
40/female
Cystic
Superior mesenteric vein,
hepatic artery
Pancreatic duct dilatation
Normal
24/male
Head
Portal vein
Normal
Abdominal pain, weight loss
48/male
Absent
Present
Present
Head
Head
Normal
Cystic
15/female
13/female
common hepatic artery,
superior mesenteric vein
Present
Cystic
Solid
58/female
Present
Upstream biliary dilatation
Abdominal pain, weight
loss, fever, night sweat
Para-pancreatic
Body and tail
Pancreatic duct and bile
ducts
None
Cystic
27/male
32/male
Cystic
Fever, weight loss
Head
29/male
50/Female
Rao et al. [90]
Head and body
Abdominal pain, jaundice,
nausea
Abdominal pain, fever, night
sweat, headache
24/male
Sonthalia et al. [46]
Head
Invasion
Nature Lymph
of mass nodes
Reference
Absent
-
-
-
-
-
-
-
-
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Pancreatic and common bile
duct dilatation
Normal
Not dilated
-
-
-
-
-
-
-
-
-
-
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as fever (unless pyogenic cholangitis develops due to
biliary duct compression) and the normal values of tumor
markers [61]. In patients without typically tuberculosis
manifestations (such as fever, night sweats, weight loss
or cough), a range of cystic pancreatic lesions, including
common lesions (pseudocysts, serous or mucinous
cystadenomas, intraductal papillary mucinous neoplasm)
and rare lesions such as solid pseudopapillary tumors
pancreatic epithelial cysts, may need to be considered
[62].
Pancreatic TB can be classified radiologically into 3
groups: mass-forming (with or without diffuse pancreatic
enlargement), a diffuse form and a small, nodular form.
The mass-forming is the most common form that accounts
for 94.4% of cases [63].
Several imaging methods like CT scan, MRI, transcutaneous
ultra-sound and endoscopic ultrasound are used to assess
pancreatic pathology. Ultra sound (US) scan is noninvasive, simple, readily available and cost-effective; thus,
it is usually used as an initial diagnostic tool. CT scan is
used to rule out associated pathologies and to plan for
disease management. It is the investigation of choice for
pathologies of pancreas because of its high sensitivity.
Although imaging findings may suggest the possibility
of tuberculosis, none of them are neither specific nor
pathognomonic for pancreatic TB [64]. They can reveal
diffuse enlargement of the pancreas [64-66], focal
hypoechoic mass on ultrasound or cystic lesions [67-73]
(mostly in the head and uncinate process), heterogeneously
hypo-isoechoic or isodense lesions on ultrasound and CT
Scan, respectively, (primarily in the head) [39, 64, 65, 67,
69, 74] and enlarged peripancreatic [67, 70, 75] and other
abdominal LNs [45, 64, 69, 70, 76, 77].
In pancreatic TB common bile duct and the pancreatic
duct appear normal in images, even if the mass is
localized centrally in the head of the pancreas. Contrary
to pancreatic TB, in pancreatic adenocarcinoma the
pancreatic duct is dilated in the tumors that are positioned
centrally in the head region. Pancreatic enlargement with
narrowing of the main pancreatic duct and heterogeneous
enhancement is the characteristic of the diffuse form of
pancreatic tuberculosis [78]. Bile cytology on endoscopic
retrograde cholangiopancreatography (ERCP) may help in
establishing the diagnosis [10, 56].
However, EUS-FNA sampling is essential for establishing
the diagnosis of pancreatic tuberculosis. The samples are
evaluated by staining, cytology, bacteriology, culture and
polymerase chain reaction assay [79-86]. A definitive
decision is usually made based on a histopathological or
microbiological examination of a specimen that is obtained
from the pancreas or based on peripancreatic LNs. In a
study, Song et al. [87] were able to diagnose pancreatic/
peri-pancreatic tuberculosis in 76.2% of patients using
EUS-FNA. The microscopic features of tuberculosis are
granuloma, caseation necrosis (seen in 75%-100% of cases)
and presence of acid fast bacilli (identified in 20%-40% of
cases) [84]. EUS is a reliable technique for differentiating
pancreatic lesion from peripheral structures [87]. It is
also preferred for tissue biopsy because of less chances of
needle tract dissemination especially when the mass seems
malignant. Rana et al. found that the majority of patients
with pancreatic tuberculosis (83.3%) had granulomas with
culture for Mycobacterium tuberculosis being positive in 1
of 2 patients (50.0%) tested and acid fast bacilli being seen
in only 1 of 6 (16.7%) [79]. In addition, acid fast bacilli
smear using auramine or Ziehl-Neelsen staining can also
be employed for this purpose.
As a result, and given the simplicity of the test and the
rapid results that it produces, EUS-FNA with an acid-fast
smear should be required for pancreatic TB diagnosis. A
PCR assay yields highly specific same-day results, when
used to detect mycobacterial DNA. Although its sensitivity
to TB in FNA specimens has not yet been established,
the PCR assay is increasingly used adjunctive to special
staining techniques and mycobacterial cultures. It may
show positive results even when specimen cultures are
negative [77].
Therefore, diagnosis is a challenge, calling for a team
approach with the goal of making the diagnosis noninvasively.
Treatment
Most cases of pancreatic TB respond well to ATD [32, 71,
88-90]. Therefore invasive treatments such as surgery and
the drainage of fluid are not necessary most of the times
[32]. Directly observed therapy with a standard multiple
ATD regimen including isoniazid, rifampicin, pyrazinamide,
and ethambutol or streptomycin for 6-12 months, is usually
effective [74]. However for those patients whose tuberculous
pancreatic mass is enlarged and causes symptoms even
after ATDs therapy for a reasonable period of time, we
should consider minimally invasive procedures [32] such
as endoscopic internal drainage, percutaneous catheter
drainage or biliary stenting. Percutaneous catheter drainage is
preferably used in patients with no pancreatic duct strictures
and pancreatic duct-pseudocyst communications and in those
with immature or infected pseudocysts, or when the patient
is at high surgical risk, or exhibits malnourishment [91,
92]. Also ATDs have hepatotoxic effects, and malnourished
patients with jaundice are at higher risk. Therefore, patients
with underlying liver disease might require modification of
ATDs [79].
Conflicting Interest
The authors had no conflicts of interest
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